Male Figs Research Articles

Assessing the Impact of Genotype-Specific Caprifig Fruit Storage on the Pollination Efficacy and Fruit Quality of “Bursa Siyahı” Cultivar: A Multivariate Analysis Approach

Fig types such as “Smyrna” and “San Pedro” require pollination (called caprification in fig cultivation) to produce a commercial crop, based on the crop and pollination characteristics of figs. Caprification is the process of hanging caprifig (male fig) fruits on female fig trees to ensure the transfer of pollen from the female fig to the caprifig by a wasp (Blastophaga psenes) that lives within the caprifig. It is necessary to extend the caprification period by using caprifig genotypes that ripen at different times, as female fig fruits ripen gradually. However, as caprifigs may not be continuously available for pollinating female figs, storing suitable caprifigs is necessary. The aim of this study was to assess changes in Blastophaga psenes, the duration of Blastophaga’s exit, and the viability of pollen from caprifigs of different genotypes (16 08 05, 16 08 09, 16 08 10, 16 09 10, and 16 ZF 08) stored for caprification. These stored caprifig genotypes were subsequently used for pollination three times at 8-day intervals, after which their impact on the set and quality of the edible fig fruits was evaluated. According to the average data, at the end of storage, the least B.psenes loss was obtained from the 16 08 05 (61.03%) genotype, and the highest was obtained from the 16 09 10 (67.00%) genotype. Pollen germination tended to increase with the storage of caprifig fruits, but this increase was not linear. After storage, the 16 08 09 and 16 09 10 genotypes exhibited greater pollen germination. The highest fruit set and quality were obtained when the 16 08 09 and 16 09 10 genotypes were used as pollen sources. Furthermore, since the 16 08 10 genotype is the latest ripening caprifig genotype, it has been determined that it can pollinate late-ripening “Bursa Siyahı” fruits. Principal component and path analysis demonstrated that pollen viability and germination rate were crucial in selecting caprifig genotypes for fruit set and quality.

Pollinator attraction in the Ficus deltoidea complex: Varietal specificity in a fig wasp that likes to stay close to home

Species boundaries are maintained by limitations on gene flow between taxa. In flowering plants pollinator specificity can strongly influence gene flow patterns and facilitate speciation. Fig trees are species rich and ecologically significant plants. It was once believed that each species had its own unique pollinator fig wasp, but numerous exceptions are now known. The dioecious Ficus deltoidea complex is distributed across southern South-East Asia with 13 recognised varieties of uncertain status, seven of which are found in Peninsular Malaysia. We investigated the host preferences of one of their Blastophaga pollinators, reared from the epiphytic F. deltoidea var. angustifolia. Our series of experimental manipulations using free-flying fig wasps and figs on host trees showed that male figs were preferred, that only their natal variety was attractive and that pollinators only dispersed from their natal trees if no suitable figs were present there. Fig wasps can only reproduce in male hosts, so preferred entry to male figs has clear advantages for them, as does their reluctance to disperse from natal trees. This behaviour is likely to reduce seed set on female plants, with potential consequences for host population dynamics. The extreme specificity of the Blastophaga sp. suggests gene flow between varieties of F. deltoidea is low or absent and that different varieties may be different biological species.

Active pollination in a functionally dioecious Ficus species: An interplay between pollinator behaviour and floral morphology

Active pollination has evolved four times in brood site pollination mutualisms. When pollination is active, the pollinator's behaviour specifically evolves to ensure flower fertilisation. In functionally dioecious Ficus species, the male figs host pollinating wasp larvae, while wasps cannot breed in the female figs because the styles are longer than the wasp ovipositor. Here we investigate the dioecious Ficus hispida. We show that in male figs, every time the wasp has laid an egg into a pistillate flower, it removes one pollen grain from its pollen pockets and places it on the hypopygium. When the wasp inserts its ovipositor into the next flower, the pollen grain is deposited deep within the style. Each ovipositor insertion results in flower pollination and insect oviposition. Because of systematic pollination of the flowers into which the eggs are laid, the wasp larvae benefit from feeding on fertilised endosperm while no seed are produced. In female figs, after probing a flower, the wasp presents pollination behaviour only every five visits. However, if it does occur, this behaviour lasts longer than in male figs and results in the deposition of on average 10 pollen grains on the hypopygium. The exposed sticky papillae on the stigmatic surface collect pollen from the hypopygium and pollen tubes may grow to neighbouring stigmas, ensuring secondary dispersal and efficient ovule fertilisation. Overall, our study demonstrates that the floral morphology of male figs facilitates precise pollen deposition, beneficial for the wasp progeny, while the floral morphology of female figs compensates for wasp pollination behaviour that is not selected in those figs. We conclude that the morphology of the arena in which interactions with its pollinator are played out is the result of selection on the plant to maximize its male and female fitness. Incidentally, this morphology stabilises the mutualistic interaction.

Genetic Diversity, Population Structure, and Association Analysis of Female and Male Fig Genotypes (Ficus carica L.)

Genetic Diversity, Population Structure, and Association Analysis of Female and Male Fig Genotypes (Ficus carica L.)

Composition Diversity and Expression Specificity of the TPS Gene Family among 24 Ficus Species

Volatile organic compounds (VOCs) released by the receptive syconia of Ficus species play a vital role in attracting highly species-specific pollinating fig wasps. The components of VOCs vary considerably among Ficus species, but are generally dominated by a few common terpenoid compounds or specific proportions of several compounds. Terpene synthase (TPS) is the main source of specific and diverse terpenoids, but the evolution of the TPS gene family in Ficus and the potential functions of the TPS genes in species-specific pollination remain largely unelucidated. In this study, using transcriptomes of ostiole bracts of receptive male figs from 24 Ficus species collected from South China and Southeast Asia, we comprehensively scanned and investigated the composition and evolutionary characteristics of all TPS genes in all 24 species. We identified 248 TPS genes, including 33 orthologous genes and six singletons. Sequence and phylogenetic analysis showed that a majority of the 248 TPSs contained the DDXXD and DTE motifs, rather than the DXDD motif, and involved all subfamilies (TPS-a,b,c,e/f and g) known in other angiosperm genomes, suggesting a very diverse and complex composition of class I TPSs during the receptive phase. In addition, compared to TPS-a, which is generally the largest subfamily in some plants, the TPS-b subfamily contained the highest number of genes in Ficus species. Expression profile comparison showed that the distribution and expression levels of different TPSs among different Ficus species differed considerably, but a few TPS genes were common across most species. Positive selection analysis showed that the Ficus TPS genes were mainly under purifying selection, with only four genes having positive selection signals and two genes having positive selection sites, and two genes having relatively fast-evolving rates. The present study demonstrates the basic evolutionary characteristics of TPS genes in Ficus and reveals the roles of TPSs in shaping the diversity and specificity of the fig–fig wasp symbiotic relationship.

Maintenance of specificity in sympatric host-specific fig/wasp pollination mutualisms.

BackgroundFig/wasp pollination mutualisms are extreme examples of species-specific plant-insect symbioses, but incomplete specificity occurs, with potentially important evolutionary consequences. Why pollinators enter alternative hosts, and the fates of pollinators and the figs they enter, are unknown.MethodsWe studied the pollinating fig wasp, Ceratosolen emarginatus, which concurrently interacts with its typical host Ficus auriculata and the locally sympatric alternative host F. hainanensis, recording frequencies of the wasp in figs of the alternative hosts. We measured ovipositor lengths of pollinators and style lengths in female and male figs in the two host species. Volatile organic compounds (VOCs) emitted by receptive figs of each species were identified using GC-MS. We tested the attraction of wasps to floral scents in choice experiments, and detected electrophysiologically active compounds by GC-EAD. We introduced C. emarginatus foundresses into figs of both species to reveal the consequences of entry into the alternative host.ResultsC. emarginatus entered a low proportion of figs of the alternative host, and produced offspring in a small proportion of them. Despite differences in the VOC profiles of the two fig species, they included shared semiochemicals. Although C. emarginatus females prefer receptive figs of F. auriculata, they are also attracted to those of F. hainanensis. C. emarginatus that entered male figs of F. hainanensis produced offspring, as their ovipositors were long enough to reach the bottom of the style; however, broods were larger and offspring smaller than in the typical host. Female figs of F. hainanensis failed to produce seeds when visited by C. emarginatus. These findings advance our current understanding of how these species-specific mutualisms usually remain stable and the conditions that allow their diversification.

Association of Fig Pollinating Wasps and Fig Nematodes inside Male and Female Figs of a Dioecious Fig Tree in Sumatra, Indonesia

Simple SummaryIt has been known that fig pollinating wasps can transfer nematodes when they enter receptive figs to deposit their eggs (male figs in male trees) and pollinate the flowers (female figs in female trees) of a dioecious fig tree. However, the fate of nematodes transferred into female figs was unknown, since the pollinating wasps that enter female figs cannot reproduce. This study examined whether the nematodes transferred by pollinating wasps into female figs of Ficus hispida could develop and reproduce in the same way as in male figs. Three species of nematodes were found to develop within the male and female figs of F. hispida, with populations peaking at about the same time for both sexes of figs. Our findings showed that the female figs could support the growth and reproduction of the three nematodes; however, there was no pollinator offspring to transfer the nematodes out of the figs. The results provide a better understanding of the development of nematodes in male and female figs of a dioecious fig tree, which may also influence the biodiversity of the tropical ecosystem.Nematodes can grow within the inflorescences of many fig trees (Ficus spp., Moraceae); however, the feeding behaviour of most nematodes is not known. Fig pollinating wasps (Hymenoptera: Agaonidae) transfer nematodes into young figs upon the wasps’ entry into the figs to deposit their eggs. Most Asian fig trees, however, are functionally dioecious, and the pollinating wasps that enter female figs are unable to reproduce. They fail to produce the offspring required to carry the new generations of nematodes. We examined whether female figs of F. hispida can nonetheless support the development of phoretic nematode populations. Nematodes were extracted from male and female figs sampled in Sumatra, Indonesia, to compare the growth of their populations within the figs. We found three species of nematodes that grew within figs of male and female trees of F. hispida: Ficophagus cf. centerae (Aphelenchoididae), Martininema baculum (Aphelenchoididae) and Caenorhabditis sp (Rhabditidae). The latter species (Caenorhabditis sp.) has never been reported to be associated with F. hispida before. Nematode populations peaked at around 120–140 individuals in both sexes of figs, at the time when a succeeding generation of adult fig wasps appeared within male figs. The female figs could support the growth and reproduction of the three nematodes species; however, the absence of vectors meant that female figs remained as traps from which there could be no escape.

Asymmetric sharing of pollinator fig wasps between two sympatric dioecious fig trees: a reflection of supply and demand or differences in the size of their figs?

BackgroundHost specificity among pollinator fig wasps (Agaonidae) depends on host plant specific volatile cues, but fig wasps must also pass through a narrow physical barrier (the ostiole) if they are to pollinate and oviposit. Across South East Asia the dioecious shrub Ficus hirta is associated with at least ten pollinator species allied to Valisia javana. Ficus triloba has a single recorded pollinator, Valisia esquirolianae. Receptive figs of F. hirta are usually much smaller than those of F. triloba, but at a mainland site where F. hirta has atypically large figs we identified both V. esquirolianae and V. javana from both Ficus species using COI and ITS2 sequencing. To investigate whether this host overlap was exceptional we reared fig wasps from the two trees elsewhere and recorded features that may facilitate host transfer between them, including attractant volatiles, reproductive phenology and the sizes of their figs and fig wasps.ResultsThe two Ficus species were found to support both Valisia species at several of the sites, suggesting that the differences we detected in volatile profiles, ostiole sizes and pollinator head sizes are not strict barriers to host sharing. Valisia javana colonised F. triloba more frequently than V. esquirolianae colonised F. hirta.ConclusionsThis asymmetric sharing of pollinators may reflect the relative abundance of the two species of fig wasps and differences in host reproductive phenology. Asynchronous flowering of individual F. hirta may favor local retention of pollinators, in contrast to the tree-wide synchrony of F. triloba figs, which can generate local shortages of V. esquirolianae. If the pollinator sharing by male figs of F. triloba and F. hirta also occurs in female figs then this could result in gene flow between them.

Analysis of Ficus hirta Fig Endosymbionts Diversity and Species Composition

Endosymbionts living in plants and insects are pervasive. Ficus (Moraceae) has very special inflorescences (which we also call figs) enclosed like an urn, and such inflorescence is usually parasitized by fig wasps. Ficus breeds fig wasp larvae in its figs and adult fig wasps pollinate for Ficus, Ficus and its obligated pollinator formed fig-fig wasp mutualism. Previous studies have found that this confined environment in figs may have provided protection for fig wasps and that this has left some imprints on the genome of fig wasps during the coevolution history of figs and fig wasps. Research on the diversity of both bacteria and fungi in figs are fewer. Our study explored the diversity of endosymbionts in Ficus hirta figs. We utilized high-throughput sequencing and biological database to identify the specific microorganism in figs, then conducted microorganism communities’ diversity analysis and function annotation analysis. As a result, we identified the dominant endosymbionts in figs, mainly some insect internal parasitic bacteria and fungi, plant pathogen, endophytes, and saprotroph. Then we also found bacteria in Ficus hirta figs were more diversified than fungi, and bacteria communities in female figs and functional male figs were different. These findings may give us more insight into the coevolution and interaction among endosymbiont, fig, and fig wasp.

AGAMOUS Gene as a New Sex-Identification Marker in Fig (Ficus carica L.) Is More Efficient Than RAN1.

Fig is an ancient gynodioecious fruit tree with females for commercial fruit production and hermaphrodites (males) sometimes used as pollen providers. An early sex-identification method would improve breeding efficiency. Three AGAMOUS (AG) genes were recruited from the Ficus carica genome using AG sequences from Ficus microcarpa and Ficus hispida. FcAG was 5230 bp in length, with 7 exons and 6 introns, and a 744-bp coding sequence. The gene was present in both female and male fig genomes, with a 15-bp deletion in the 7th exon. The other two AG genes (FcAG2-Gall_Stamen and FcAG3-Gall_Stamen) were male-specific, without the 15-bp deletion (759-bp coding sequence), and were only expressed in the gall and stamen of the male fig fruit. Using the deletion as the forward primer (AG-Marker), male plants were very efficiently identified by the presence of a 146-bp PCR product. The previously reported fig male and female polymorphism gene RESPONSIVE-TO-ANTAGONIST1 (RAN1) was also cloned and compared between male and female plants. Fifteen SNPs were found in the 3015-bp protein-coding sequence. Among them, 12 SNPs were identified as having sex-differentiating capacity by checking the sequences of 27 known male and 24 known female cultivars. A RAN1-Marker of 608 bp, including 6 SNPs, was designed, and a PCR and sequencing-based method was verified with 352 fig seedlings from two hybrid populations. Our results confirmed that the newly established AG-Marker is as accurate as the RAN1-Marker, and provide new clues to understanding Ficus sex determination.

Sky islands as foci for divergence of fig trees and their pollinators in southwest China.

The dynamics of populations and their divergence over time have shaped current levels of biodiversity and in the case of the "sky islands" of mountainous southwest (SW) China have resulted in an area of exceptional botanical diversity. Ficus tikoua is a prostrate fig tree subendemic to the area that displays unique intraspecific diversity, producing figs typical of different pollination modes in different parts of its range. By combining climate models, genetic variation in populations of the tree's obligate fig wasp pollinators and distributions of the different plant phenotypes, we examined how this unusual situation may have developed. We identified three genetically distinct groups of a single Ceratosolen pollinator species that have largely parapatric distributions. The complex topography of the region contributed to genetic divergence among the pollinators by facilitating geographical isolation and providing refugia. Migration along elevations in response to climate oscillations further enhanced genetic differentiation of the three pollinator groups. Their distributions loosely correspond to the distributions of the functionally significant morphological differences in the male figs of their host plants, but postglacial expansion of one group has not been matched by spread of its associated plant phenotype, possibly due to a major river barrier. The results highlight how interplay between the complex topography of the "sky island" complex and climate change has shaped intraspecies differentiation and relationships between the plant and its pollinator. Similar processes may explain the exceptional botanical diversity of SW China.

Differentiation during fig ontogeny suggests opposing selection by mutualists.

Dioecy allows separation of female and male functions and therefore facilitates separate co‐evolutionary pathways with pollinators and seed dispersers. In monoecious figs, pollinators' offspring develop inside the syconium by consuming some of the seeds. Flower‐stage syconia must attract pollinators, then ripen and attract seed dispersers. In dioecious figs, male (“gall”) figs produce pollen but not viable seeds, as the pollinators' larvae eat all seeds, while female (“seed”) figs produce mostly viable seeds, as pollinators cannot oviposit in the ovules. Hence, gall and seed figs are under selection to attract pollinators, but only seed figs must attract seed dispersers. We test the hypothesis that seed and gall syconia at the flower stage will be similar, while at the fruiting stage they will differ. Likewise, monoecious syconia will be more similar to seed than gall figs because they must attract both pollinators and seed dispersers. We quantified syconium characteristics for 24 dioecious and 11 monoecious fig species and recorded frugivore visits. We show that seed and gall syconia are similar at the flower stage but differ at the fruit stage; monoecious syconia are more similar to seed syconia than they are to gall syconia; seed and gall syconia differentiate through their ontogeny from flower to fruit stages; and frugivores visit more monoecious and seed syconia than gall syconia. We suggest that similarity at the flower stage likely enhances pollination in both seed and gall figs and that differentiation after pollination likely enhances attractiveness to seed dispersers of syconia containing viable seeds. These ontogenetic differences between monoecious and dioecious species provide evidence of divergent responses to selection by pollinators and seed dispersers.

Differential deployment of sanctioning mechanisms by male and female host trees in a gynodioecious fig-wasp mutualism.

In some insect nursery pollination mutualisms, plant hosts impose net costs to uncooperative "cheater" symbionts. These "sanctions" promote mutualism stability but their precise adaptive nature remains unclear. In fig-wasp mutualisms host trees (Ficus spp.) are only pollinated by female agaonid wasps whose larvae only use galled fig flowers as food. In actively pollinated systems, if wasps fail to pollinate, sanctions can result via fig abortion, killing all wasp offspring, or by increased offspring mortality within un-aborted figs. These sanctions result from selective investment to pollinated inflorescences, a mechanism present in almost all angiosperms. To more fully understand how selective investment functions as sanctions requires the measurement of variation in their costs and benefits to both hosts and symbionts. Gynodioecious fig-tree-fig-wasp mutualisms are particularly suitable for this because pollen and wasps are produced only in the figs of "male" trees and seeds only in the figs of "female" trees. Male and female trees thus incur different net costs of pollen absence, and costs of sanctions to pollen-free "cheater" wasps only occur in male trees. We used the actively pollinated host tree Ficus hispida and introduced into male and female figs either 1, 3, 5, 7, or 9 all pollen-laden "cooperative" (P+) or all pollen-free "cheater" (P-) wasps. Abortion in both male and female trees was highest in P- figs, with P- fig abortion higher in females (~90%) than in males (~40%). Fig abortion was negatively associated with foundress number mainly in P+ figs; in P- figs abortion was only weakly associated with the number of "cheater" wasps, especially in female figs. In un-aborted male figs, wasp offspring mortality was higher in P- figs than in P+ figs, and in P- figs correlated positively with foundress (cheater) number. Increased offspring mortality was biased against female wasp offspring and likely resulted from reduced larval nutrition in unpollinated flowers. Variation in selective investment to P- figs thus reflects costs and benefits of pollen absence/presence to hosts, variation that translates directly to net costs to cheater wasps.

A new species of Megaselia Rondani (Diptera: Phoridae) associated with one sex of a dioecious fig tree in Thailand

Megaselia ischnopodae Disney n. sp. (Diptera, Phoridae) is reared from larvae found in mature male figs of Ficus ischnopoda Miq. (Urticales, Moracea) in Thailand. Other phorid species associated with fig trees are briefly reviewed.

A new species of Silba (Diptera; Lonchaeidae) associated with figs.

A new species of Silba Macquart 1851, Silba ischnopoda sp. nov., is described from Thailand and Cambodia. The Thailand individuals were obtained from larvae found in mature male figs of the dioecious Ficus ischnopoda Miq. Comparisons are made with other similar Asian Silba species which have also been reared from the figs of Ficus species. Male figs support development of fig wasp larvae, not seeds, suggesting that the larvae of S. ischnopoda may be predaceous.

Style length variation in male and female figs: development, inheritance, and control of pollinator oviposition

AbstractFig trees (Ficus spp., Moraceae) depend on female fig wasps to transport their pollen and as a reward provide nutrition for pollinator fig wasp larvae. Most pollinators are host specific, but natural plant hybrids occur if atypical hosts are pollinated. Female fig wasps lay their eggs into ovaries of female flowers in receptive figs by inserting their ovipositors through the styles, and relative style and ovipositor lengths are believed to largely determine their ability to oviposit. In dioecious fig trees, flowers in receptive male figs have short styles and support larval development, whereas flowers in receptive female figs have long styles and only develop into seeds. Using the dioecious fig tree species Ficus montana Burm. f. and Ficus asperifolia Miq., we recorded the comparative ontogeny of style lengths to determine whether style growth in the two sexes is coordinated with the attraction of pollinators, and how maximum style lengths relate to the ovipositor lengths of their pollinators. F1 hybrids between these species produce viable seeds, but no pollinator offspring. We examined style lengths in F1s and backcrosses, relative to those of their parents, and whether coordination of style growth with pollinator attraction is disrupted. The ovipositor of Kradibia tentacularis (Grandi) (Hymenoptera: Agaonidae), the pollinator of F. montana, could reach some of the ovaries in female figs, but fails to lay eggs there. Styles in male F1 figs were intermediate in length between those of the two parents, but in female F1 figs styles grew longer than in either parent. Maximum style lengths in F1s were partially decoupled from receptivity, especially in female figs. Our results illustrate how timing of stigmal growth is coordinated with pollinator attraction, and that this coordination can be disrupted in hybrid individuals.

Floral constraint resulting from intersexual mimicry in a gynodioecious fig tree

Fig trees (Ficus: Moraceae) are pollinated by female fig wasps (Agaonidae) whose larvae develop inside galled flowers of unusual inflorescences (figs). Most fig trees also support communities of non-pollinating fig wasps. Figs of different species display great size variation and contain tens to tens of thousands of flowers. Around one-half the species of fig trees have the gynodioecious breeding system, where female trees have figs that produce seeds and male trees have figs that support development of pollinators. Mutual mimicry between receptive male and female figs ensures that pollinators enter female figs, even though the insects will die without reproducing, but the need to give no sex-specific cues to the pollinators may constrain differences in size between receptive male and female figs. We compared relationships between inflorescence size and some measures of reproductive success in male and female figs of Ficus montana grown under controlled conditions in the presence of the pollinator Kradibia tentacularis and its main parasitoid Sycoscapter sp. indesc. Female figs that contained more flowers produced more seeds, but male figs did not increase the production of female pollinator K. tentacularis fig wasps in proportion of the flower number. Although more flowers were galled by the pollinators in male figs containing more female flowers, the high larval mortality caused by parasitism and nutritional limitation prevented the increase in the production of adult female offspring. Selection may favor the increase in flower numbers within figs in female plants of F. montana, but contrarily constrain this attribute in male plants.

Seasonality of Leaf and Fig Production in Ficus squamosa, a Fig Tree with Seeds Dispersed by Water.

The phenology of plants reflects selection generated by seasonal climatic factors and interactions with other plants and animals, within constraints imposed by their phylogenetic history. Fig trees (Ficus) need to produce figs year-round to support their short-lived fig wasp pollinators, but this requirement is partially de-coupled in dioecious species, where female trees only develop seeds, not pollinator offspring. This allows female trees to concentrate seed production at more favorable times of the year. Ficus squamosa is a riparian species whose dispersal is mainly by water, rather than animals. Seeds can float and travel in long distances. We recorded the leaf and reproductive phenology of 174 individuals for three years in Chiang Mai, Northern Thailand. New leaves were produced throughout the year. Fig production occurred year-round, but with large seasonal variations that correlated with temperature and rainfall. Female and male trees initiated maximal fig crops at different times, with production in female trees confined mainly to the rainy season and male figs concentrating fig production in the preceding months, but also often bearing figs continually. Ficus squamosa concentrates seed production by female plants at times when water levels are high, favouring dispersal by water, and asynchronous flowering within male trees allow fig wasps to cycle there, providing them with potential benefits by maintaining pollinators for times when female figs become available to pollinate.

Extremely high proportions of male flowers and geographic variation in floral ratios within male figs of Ficus tikoua despite pollinators displaying active pollen collection.

Most plants are pollinated passively, but active pollination has evolved among insects that depend on ovule fertilization for larval development. Anther-to-ovule ratios (A/O ratios, a coarse indicator of pollen-to-ovule ratios) are strong indicators of pollination mode in fig trees and are consistent within most species. However, unusually high values and high variation of A/O ratios (0.096-10.0) were detected among male plants from 41 natural populations of Ficus tikoua in China. Higher proportions of male (staminate) flowers were associated with a change in their distribution within the figs, from circum-ostiolar to scattered. Plants bearing figs with ostiolar or scattered male flowers were geographically separated, with scattered male flowers found mainly on the Yungui Plateau in the southwest of our sample area. The A/O ratios of most F.tikoua figs were indicative of passive pollination, but its Ceratosolen fig wasp pollinator actively loads pollen into its pollen pockets. Additional pollen was also carried on their body surface and pollinators emerging from scattered-flower figs had more surface pollen. Large amounts of pollen grains on the insects' body surface are usually indicative of a passive pollinator. This is the first recorded case of an actively pollinated Ficus species producing large amounts of pollen. Overall high A/O ratios, particularly in some populations, in combination with actively pollinating pollinators, may reflect a response by the plant to insufficient quantities of pollen transported in the wasps' pollen pockets, together with geographic variation in this pollen limitation. This suggests an unstable scenario that could lead to eventual loss of wasp active pollination behavior.

Sexual specialization in phenology in dioecious Ficus benguetensis and its consequences for the mutualism.

BackgroundTiming of reproductive events has become central in ecological studies linking success in pollination and seed dispersion to optimizing the probability and periods of encounters with pollinators or dispersers. Obligate plant–insect interactions, especially Ficus–fig wasp mutualisms, offer striking examples of fine-tuned encounter optimization as biological cycles between mutualistic partners are deeply dependent on each other and intertwined over generations. Despite fig flowering phenology being crucial in maintaining Ficus–fig wasp mutualisms, until now, the forces of selection shaping the phenological evolution of dioecious fig trees have received little attention. By conducting a 2-year survey of a population of Ficus benguetensis in Northern Taiwan, we assessed whether environmental factors or other selective pressures shape the phenology of male and female fig trees.ResultsConstraints by mutualistic pollinating wasps and seed dispersers, rather than climatic factors, appeared to mainly shape fig phenology and allometry in F. benguetensis. We identified a new sexual specialization in dioecious fig trees: the position of fig production. We propose that the continuous male fig production on tree trunks can enhance the survival of pollinating fig wasps through faster localization of receptive figs while reducing the mutualistic conflict between the fig and its obligate pollinators. By contrast, in female trees, fig production is massive in summer, located on the twigs of the foliar crown and seem more related to seed dispersal and germination.ConclusionsIdentifying variations in the allometry and phenology of dioecious figs provide valuable insights into how monoecious and dioecious species resolve mutualism conflicts and into the emergence of dioecy in fig trees.Electronic supplementary materialThe online version of this article (doi:10.1186/s40529-015-0113-7) contains supplementary material, which is available to authorized users.